DNA duplexes exist as dynamic ensembles of interconverting conformations in solution. Conventional nuclear magnetic resonance (NMR) data interpretation often simplifies this behavior by assuming one dominant structure, but multiple substates (such as different backbone conformers) can coexist. Here, we present an approach that refines the interpretation of 31P NMR data in the Dickerson-Drew DNA by integrating a nucleotide conformational classification (NtC) (Černý et al., Nucleic Acids Research 2020, 48, 6367-6381) with molecular dynamics (MD) simulations. By finely classifying backbone conformers into distinct NtC-defined states and using MD to predict their populations, we achieve a more nuanced correspondence between experimental NMR observables and DNA structure-dynamical heterogeneity. Application of this framework demonstrates a radical improvement of NMR data interpretation, thereby enhancing the reliability of deducing DNA conformational equilibria in solution.

Department of Physical Chemistry Faculty of Science Palacký University Olomouc 77146 Olomouc Czech Republic

Institute of Organic Chemistry and Biochemistry Czech Academy of Sciences 166 10 Praha 6 Czech Republic

J Heyrovský Institute of Physical Chemistry Czech Academy of Sciences 182 00 Prague 8 Czech Republic

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Schroeder S. A., Roongta V., Fu J. M., Jones C. R., Gorenstein D. G.. Sequence-Dependent Variations in the P-31 Nmr-Spectra and Backbone Torsional Angles of Wild-Type and Mutant Lac Operator Fragments. Biochemistry-Us. 1989;28(21):8292–8303. doi: 10.1021/bi00447a006. PubMed DOI

Reddy S. Y., Obika S., Bruice T. C.. Conformations and dynamics of Ets-1 ETS domain-DNA complexes. P Natl. Acad. Sci. USA. 2003;100(26):15475–15480. doi: 10.1073/pnas.1936251100. PubMed DOI PMC

Wellenzohn B., Flader W., Winger R. H., Hallbrucker A., Mayer E., Liedl K. R.. Exocyclic groups in the minor groove influence the backbone conformation of DNA. Nucleic Acids Res. 2001;29(24):5036–5043. doi: 10.1093/nar/29.24.5036. PubMed DOI PMC

van Dam L., Korolev N., Nordenskiöld L.. Polyamine-nucleic acid interactions and the effects on structure in oriented DNA fibers. Nucleic Acids Res. 2002;30(2):419–428. doi: 10.1093/nar/30.2.419. PubMed DOI PMC

Hartmann B., Piazzola D., Lavery R.. B-I-B-Ii Transitions in B-DNA. Nucleic Acids Res. 1993;21(3):561–568. doi: 10.1093/nar/21.3.561. PubMed DOI PMC

Schwieters C. D., Clore G. M.. A physical picture of atomic motions within the Dickerson DNA dodecamer in solution derived from joint ensemble refinement against NMR and large-angle X-ray scattering data. Biochemistry-Us. 2007;46(5):1152–1166. doi: 10.1021/bi061943x. PubMed DOI

Heddi B., Foloppe N., Bouchemal N., Hantz E., Hartmann B.. Quantification of DNA BI/BII backbone states in solution. Implications for DNA overall structure and recognition. J. Am. Chem. Soc. 2006;128(28):9170–9177. doi: 10.1021/ja061686j. PubMed DOI

Ben Imeddourene A., Elbahnsi A., Guéroult M., Oguey C., Foloppe N., Hartmann B.. Simulations Meet Experiment to Reveal New Insights into DNA Intrinsic Mechanics. PLoS Comput. Biol. 2015;11:e1004631. doi: 10.1371/journal.pcbi.1004631. PubMed DOI PMC

Schneider B., Božíková P., Nečasová I., Čech P., Svozil D., Černý J.. A DNA structural alphabet provides new insight into DNA flexibility. Acta Crystallogr. Sect. D-Struct. Biol. 2018;74:52–64. doi: 10.1107/S2059798318000050. PubMed DOI PMC

Hartmann B., Lavery R.. DNA structural forms. Q. Rev. Biophys. 1996;29(4):309–368. doi: 10.1017/S0033583500005874. PubMed DOI

Zubova E. A., Strelnikov I. A.. Experimental detection of conformational transitions between forms of DNA: problems and prospects. Biophysical Reviews. 2023;15:1053–1078. doi: 10.1007/s12551-023-01143-9. PubMed DOI PMC

Černý J., Božíková P., Svoboda J., Schneider B.. A unified dinucleotide alphabet describing both RNA and DNA structures. Nucleic Acids Res. 2020;48(11):6367–6381. doi: 10.1093/nar/gkaa383. PubMed DOI PMC

Černý J., Božíková P., Malý M., Tykač M., Biedermannová L., Schneider B.. Structural alphabets for conformational analysis of nucleic acids available at dnatco.datmos.org. Acta Crystallogr. Sect. D-Struct. Biol. 2020;76:805–813. doi: 10.1107/S2059798320009389. PubMed DOI PMC

Černý J., Božíková P., Schneider B.. DNATCO: assignment of DNA conformers at dnatco.org. Nucleic Acids Res. 2016;44(W1):W284–W287. doi: 10.1093/nar/gkw381. PubMed DOI PMC

Anderson C. F., Record M. T.. Salt Nucleic-Acid Interactions. Annu. Rev. Phys. Chem. 1995;46:657–700. doi: 10.1146/annurev.pc.46.100195.003301. PubMed DOI

Sharp K. A., Honig B.. Salt Effects on Nucleic-Acids. Curr. Opin Struc Biol. 1995;5(3):323–328. doi: 10.1016/0959-440X(95)80093-X. PubMed DOI

Lankaš F., Šponer J., Hobza P., Langowski J. J.. Sequence-dependent elastic properties of DNA. J. Mol. Biol. 2000;299(3):695–709. doi: 10.1006/jmbi.2000.3781. PubMed DOI

Lavery R., Zakrzewska K., Beveridge D., Bishop T. C., Case D. A., Cheatham T., Dixit S., Jayaram B., Lankaš F., Laughton C.. et al. A systematic molecular dynamics study of nearest-neighbor effects on base pair and base pair step conformations and fluctuations in B-DNA. Nucleic Acids Res. 2010;38(1):299–313. doi: 10.1093/nar/gkp834. PubMed DOI PMC

Cheng Y. H., Korolev N., Nordenskiöld L.. Similarities and differences in interaction of K and Na with condensed ordered DNA.: A molecular dynamics computer simulation study. Nucleic Acids Res. 2006;34(2):686–696. doi: 10.1093/nar/gkj434. PubMed DOI PMC

Lavery R., Maddocks J. H., Pasi M., Zakrzewska K.. Analyzing ion distributions around DNA. Nucleic Acids Res. 2014;42(12):8138–8149. doi: 10.1093/nar/gku504. PubMed DOI PMC

Pasi M., Maddocks J. H., Lavery R.. Analyzing ion distributions around DNA: sequence-dependence of potassium ion distributions from microsecond molecular dynamics. Nucleic Acids Res. 2015;43(4):2412–2423. doi: 10.1093/nar/gkv080. PubMed DOI PMC

Musselman C. A., Kutateladze T. G.. Visualizing Conformational Ensembles of the Nucleosome by NMR. ACS Chem. Biol. 2022;17(3):495–502. doi: 10.1021/acschembio.1c00954. PubMed DOI PMC

Oh K. I., Kim J., Park C. J., Lee J. H.. Dynamics Studies of DNA with Non-canonical Structure Using NMR Spectroscopy. Int. J. Mol. Sci. 2020;21(8):2673. doi: 10.3390/ijms21082673. PubMed DOI PMC

Wijmenga S. S., van Buuren B. N. M.. The use of NMR methods for conformational studies of nucleic acids. Prog. Nucl. Magn. Reson. Spectrosc. 1998;32:287–387. doi: 10.1016/S0079-6565(97)00023-X. DOI

Williams B., Zhao B., Tandon A., Ding F., Weeks K. M., Zhang Q., Dokholyan N. V.. Structure modeling of RNA using sparse NMR constraints. Nucleic Acids Res. 2017;45(22):12638–12647. doi: 10.1093/nar/gkx1058. PubMed DOI PMC

Berman H. M., Westbrook J., Feng Z., Gilliland G., Bhat T. N., Weissig H., Shindyalov I. N., Bourne P. E.. The Protein Data Bank. Nucleic Acids Res. 2000;28(1):235–242. doi: 10.1093/nar/28.1.235. PubMed DOI PMC

Kaupp, M. ; Malkin, V. G. . Special Issue:Quantum Chemical Calculations of NMR and EPR Parameters - Foreword. In Journal of Computational Chemistry; Wiley: 1999; Vol. 20(12) pp v–vii.

Kaupp, M. ; Vaara, J. ; Munzarova, M. ; Malkina, O. L. ; Malkin, V. G. . Density Functional Calculations of NMR and EPR Parameters for Heavy-Element Compounds. In Book of Abstracts; American Chemical Society, 2000; Vol. 219, p U590.

Cheatham T. E., Young M. A.. Molecular dynamics simulation of nucleic acids: Successes, limitations, and promise. Biopolymers. 2000;56(4):232–256. doi: 10.1002/1097-0282(2000)56:4<232::AID-BIP10037>3.0.CO;2-H. PubMed DOI

Liu C., Li Y., Han B. Y., Gong L. D., Lu L. N., Yang Z. Z., Zhao D. X.. Development of the ABEEMσπ Polarization Force Field for Base Pairs with Amino Acid Residue Complexes. J. Chem. Theory Comput. 2017;13(5):2098–2111. doi: 10.1021/acs.jctc.6b01206. PubMed DOI

Calcagno F., Maryasin B., Garavelli M., Avagliano D., Rivalta I.. Modeling solvent effects and convergence of 31P-NMR shielding calculations with COBRAMM. J. Comput. Chem. 2024;45:1562–1575. doi: 10.1002/jcc.27338. PubMed DOI

Colherinhas G., Oliveira L. B. A., Castro M. A., Fonseca T. L., Coutinho K., Canuto S.. On the calculation of magnetic properties of nucleic acids in liquid water with the sequential QM/MM method. J. Mol. Liq. 2019;294:111611. doi: 10.1016/j.molliq.2019.111611. DOI

Szántó J. K., Dietschreit J. C. B., Shein M., Schütz A. K., Ochsenfeld C.. Systematic QM/MM Study for Predicting 31P NMR Chemical Shifts of Adenosine Nucleotides in Solution and Stages of ATP Hydrolysis in a Protein Environment. J. Chem. Theory Comput. 2024;20:2433–2444. doi: 10.1021/acs.jctc.3c01280. PubMed DOI PMC

Maste S., Sharma B., Pongratz T., Grabe B., Hiller W., Erlach M. B., Kremer W., Kalbitzer H. R., Marx D., Kast S. M.. The accuracy limit of chemical shift predictions for species in aqueous solution. Phys. Chem. Chem. Phys. 2024;26(7):6386–6395. doi: 10.1039/D3CP05471C. PubMed DOI

Ketzel A. F., Li X. L., Kaupp M., Sun H., Schattenberg C. J.. Benchmark of Density Functional Theory in the Prediction of C Chemical Shielding Anisotropies for Anisotropic Nuclear Magnetic Resonance-Based Structural Elucidation. J. Chem. Theory Comput. 2025;21:871–885. doi: 10.1021/acs.jctc.4c01407. PubMed DOI PMC

Přecechtělová J., Munzarová M. L., Novák P., Sklenář V.. Relationships between P chemical shift tensors and conformation of nucleic acid backbone:: A DFT study. J. Phys. Chem. B. 2007;111(10):2658–2667. doi: 10.1021/jp0668652. PubMed DOI

Přecechtělová J., Munzarová M. L., Vaara J., Novotný J., Dračínský M., Sklenář V.. Toward Reproducing Sequence Trends in Phosphorus Chemical Shifts for Nucleic Acids by MD/DFT Calculations. J. Chem. Theory Comput. 2013;9(3):1641–1656. doi: 10.1021/ct300488y. PubMed DOI

Přecechtělová J., Novák P., Munzarová M. L., Kaupp M., Sklenář V.. Phosphorus Chemical Shifts in a Nucleic Acid Backbone from Combined Molecular Dynamics and Density Functional Calculations. J. Am. Chem. Soc. 2010;132(48):17139–17148. doi: 10.1021/ja104564g. PubMed DOI

Přecechtělová J., Padrta P., Munzarová M. L., Sklenář V.. P chemical shift tensors for canonical and non-canonical conformations of nucleic acids:: A DFT study and NMR implications. J. Phys. Chem. B. 2008;112(11):3470–3478. doi: 10.1021/jp076073n. PubMed DOI

Přecechtělová J. P., Mládek A., Zapletal V., Hritz J.. Quantum Chemical Calculations of NMR Chemical Shifts in Phosphorylated Intrinsically Disordered Proteins. J. Chem. Theory Comput. 2019;15(10):5642–5658. doi: 10.1021/acs.jctc.8b00257. PubMed DOI

Benda L., Schneider B., Sychrovský V.. Calculating the Response of NMR Shielding Tensor σ­(P) and 2J­(P,C) Coupling Constants in Nucleic Acid Phosphate to Coordination of the Mg Cation. J. Phys. Chem. A. 2011;115(11):2385–2395. doi: 10.1021/jp1114114. PubMed DOI

Benda L., Vokáčová Z. S., Straka M., Sychrovský V.. Correlating the 31P NMR Chemical Shielding Tensor and the 2J­(P,C) Spin-Spin Coupling Constants with Torsion Angles ζ and α in the Backbone of Nucleic Acids. J. Phys. Chem. B. 2012;116(12):3823–3833. doi: 10.1021/jp2099043. PubMed DOI

Vokáčová Z., Buděšínský M., Rosenberg I., Schneider B., Šponer J., Sychrovský V.. Structure and Dynamics of the ApA, ApC, CpA, and CpC RNA Dinucleoside Monophosphates Resolved with NMR Scalar Spin-Spin Couplings. J. Phys. Chem. B. 2009;113(4):1182–1191. doi: 10.1021/jp809762b. PubMed DOI

Fukal J., Buděšínský M., Páv O., Jurečka P., Zgarbová M., Šebera J., Sychrovský V.. The Ad-MD method to calculate NMR shift including effects due to conformational dynamics: The P-31 NMR shift in DNA. J. Comput. Chem. 2022;43(2):132–143. doi: 10.1002/jcc.26778. PubMed DOI

Fukal J., Zgarbová M., Jurečka P., Šebera J., Sychrovský V.. Probabilistic Interpretation of NMR J-Couplings Determines BI-BII State Equilibria in DNA. J. Chem. Theory Comput. 2022;18(11):6989–6999. doi: 10.1021/acs.jctc.2c00733. PubMed DOI

Fukal J., Páv O., Buděšínský M., Šebera J., Sychrovský V.. The benchmark of 31P NMR parameters in phosphate: a case study on structurally constrained and flexible phosphate. Phys. Chem. Chem. Phys. 2017;19(47):31830–31841. doi: 10.1039/C7CP06969C. PubMed DOI

Ulyanov N. B., James T. L.. Statistical analysis of DNA duplex structural features. Method Enzymol. 1995;261:90–120. doi: 10.1016/S0076-6879(95)61006-5. PubMed DOI

Lam S. L., Chi L. M.. Use of chemical shifts for structural studies of nucleic acids. Prog. Nucl. Mag Res. Sp. 2010;56(3):289–310. doi: 10.1016/j.pnmrs.2010.01.002. PubMed DOI

Gorenstein D. G.. Conformation and dynamics of DNA and protein-DNA complexes by 31P NMR. Chem. Rev. 1994;94(5):1315–1338. doi: 10.1021/cr00029a007. DOI

Warhaut S., Mertinkus K. R., Höllthaler P., Fürtig B., Heilemann M., Hengesbach M., Schwalbe H.. Ligand-modulated folding of the full-length adenine riboswitch probed by NMR and single-molecule FRET spectroscopy. Nucleic Acids Res. 2017;45(9):5512–5522. doi: 10.1093/nar/gkx110. PubMed DOI PMC

Nielsen G., Schwalbe H.. Protein NMR spectroscopy: Hydrogen bonds under pressure. Nat. Chem. 2012;4(9):693–695. doi: 10.1038/nchem.1443. PubMed DOI

Ardenkjaer-Larsen J. H., Boebinger G. S., Comment A., Duckett S., Edison A. S., Engelke F., Griesinger C., Griffin R. G., Hilty C., Maeda H.. et al. Facing and Overcoming Sensitivity Challenges in Biomolecular NMR Spectroscopy. Angew. Chem. Int. Edit. 2015;54(32):9162–9185. doi: 10.1002/anie.201410653. PubMed DOI PMC

Cesari A., Gil-Ley A., Bussi G.. Combining Simulations and Solution Experiments as a Paradigm for RNA Force Field Refinement. J. Chem. Theory Comput. 2016;12(12):6192–6200. doi: 10.1021/acs.jctc.6b00944. PubMed DOI

Das A. K., Tuckerman M. E., Kirmizialtin S.. HB-CUFIX: Force field for accurate RNA simulations. J. Chem. Phys. 2025;162:200901. doi: 10.1063/5.0249905. PubMed DOI

Wu Z. G., Delaglio F., Tjandra N., Zhurkin V. B., Bax A.. Overall structure and sugar dynamics of a DNA dodecamer from homoand heteronuclear dipolar couplings and P-31 chemical shift anisotropy. J. Biomol. NMR. 2003;26(4):297–315. doi: 10.1023/A:1024047103398. PubMed DOI

Berendsen H. J. C., Grigera J. R., Straatsma T. P.. The missing term in effective pair potentials. J. Phys. Chem. 1987;91(24):6269–6271. doi: 10.1021/j100308a038. DOI

Joung I. S., Cheatham T. E.. Determination of alkali and halide monovalent ion parameters for use in explicitly solvated biomolecular simulations. J. Phys. Chem. B. 2008;112(30):9020–9041. doi: 10.1021/jp8001614. PubMed DOI PMC

Joung I. S., Cheatham T. E.. Molecular dynamics simulations of the dynamic and energetic properties of alkali and halide ions using water-model-specific ion parameters. J. Phys. Chem. B. 2009;113(40):13279–13290. doi: 10.1021/jp902584c. PubMed DOI PMC

Case D. A., Cheatham T.E. 3rd, Darden T., Gohlke H., Luo R., Merz K.M. Jr., Onufriev A., Simmerling C., Wang B., Woods R. J.. The Amber biomolecular simulation programs. J. Comput. Chem. 2005;26(16):1668–1688. doi: 10.1002/jcc.20290. PubMed DOI PMC

Zgarbová M., Otyepka M., Šponer J., Lankaš F., Jurečka P.. Base Pair Fraying in Molecular Dynamics Simulations of DNA and RNA. J. Chem. Theory Comput. 2014;10(8):3177–3189. doi: 10.1021/ct500120v. PubMed DOI

Zgarbová M., Šponer J., Jurečka P.. Z-DNA as a Touchstone for Additive Empirical Force Fields and a Refinement of the Alpha/Gamma DNA Torsions for AMBER. J. Chem. Theory Comput. 2021;17(10):6292–6301. doi: 10.1021/acs.jctc.1c00697. PubMed DOI

Ivani I., Dans P. D., Noy A., Pérez A., Faustino I., Hospital A., Walther J., Andrio P., Goñi R., Balaceanu A.. et al. Parmbsc1: a refined force field for DNA simulations. Nat. Methods. 2016;13(1):55–58. doi: 10.1038/nmeth.3658. PubMed DOI PMC

Becke A. D.. Density-functional thermochemistry. 3. The role of exact exchange. J. Chem. Phys. 1993;98(7):5648–5652. doi: 10.1063/1.464913. DOI

Lee C. T., Yang W. T., Parr R. G.. Development of the Colle-Salvetti correlation-energy formula into a functional of the electron-density. Phys. Rev. B. 1988;37(2):785–789. doi: 10.1103/PhysRevB.37.785. PubMed DOI

Vosko S. H., Wilk L., Nusair M.. Accurate spin-dependent electron liquid correlation energies for local spin-density calculations - a critical analysis. Can. J. Phys. 1980;58(8):1200–1211. doi: 10.1139/p80-159. DOI

Stephens P. J., Devlin F. J., Chabalowski C. F., Frisch M. J.. Ab-Initio Calculation of Vibrational Absorption and Circular-Dichroism Spectra Using Density-Functional Force-Fields. J. Phys. Chem. 1994;98(45):11623–11627. doi: 10.1021/j100096a001. DOI

Hariharan P. C., Pople J. A.. The influence of polarization functions on molecular-orbital hydrogenation energies. Theor. Chim. Acta. 1973;28(3):213–222. doi: 10.1007/BF00533485. DOI

Krishnan R., Binkley J. S., Seeger R., Pople J. A.. Self-consistent molecular-orbital methods. 20. A basis set for correlated wave-functions. J. Chem. Phys. 1980;72(1):650–654. doi: 10.1063/1.438955. DOI

Francl M. M., Pietro W. J., Hehre W. J., Binkley J. S., Gordon M. S., Defrees D. J., Pople J. A.. Self-consistent molecular-orbital methods. 23. A polarization-type basis set for 2nd-row elements. J. Chem. Phys. 1982;77(7):3654–3665. doi: 10.1063/1.444267. DOI

Clark T., Chandrasekhar J., Spitznagel G. W., Schleyer P. V.. Efficient diffuse function-augmented basis sets for anion calculations. III. The 3–21+G basis set for first-row elements, Li-F. J. Comput. Chem. 1983;4(3):294–301. doi: 10.1002/jcc.540040303. DOI

Gill P. M. W., Johnson B. G., Pople J. A., Frisch M. J.. The performance of the Becke-Lee-Yang-Parr (B-LYP) density functional theory with various basis-sets. Chem. Phys. Lett. 1992;197(4–5):499–505. doi: 10.1016/0009-2614(92)85807-M. DOI

Marenich A. V., Cramer C. J., Truhlar D. G.. Universal solvation model based on solute electron density and on a continuum model of the solvent defined by the bulk dielectric constant and atomic surface tensions. J. Phys. Chem. B. 2009;113(18):6378–6396. doi: 10.1021/jp810292n. PubMed DOI

Sychrovský V., Grafenstein J., Cremer D.. Nuclear magnetic resonance spin-spin coupling constants from coupled perturbed density functional theory. J. Chem. Phys. 2000;113(9):3530–3547. doi: 10.1063/1.1286806. DOI

Helgaker T., Watson M., Handy N. C.. Analytical calculation of nuclear magnetic resonance indirect spin-spin coupling constants at the generalized gradient approximation and hybrid levels of density-functional theory. J. Chem. Phys. 2000;113(21):9402–9409. doi: 10.1063/1.1321296. DOI

Jensen F.. The optimum contraction of basis sets for calculating spin-spin coupling constants. Theor. Chem. Acc. 2010;126(5–6):371–382. doi: 10.1007/s00214-009-0699-5. DOI

Ditchfield R.. Self-Consistent Perturbation-Theory of Diamagnetism 0.1. Gauge-Invariant Lcao Method for Nmr Chemical-Shifts. Mol. Phys. 1974;27(4):789–807. doi: 10.1080/00268977400100711. DOI

Wolinski K., Hinton J. F., Pulay P.. Efficient Implementation of the Gauge-Independent Atomic Orbital Method for Nmr Chemical-Shift Calculations. J. Am. Chem. Soc. 1990;112(23):8251–8260. doi: 10.1021/ja00179a005. DOI

Cheeseman J. R., Trucks G. W., Keith T. A., Frisch M. J.. A comparison of models for calculating nuclear magnetic resonance shielding tensors. J. Chem. Phys. 1996;104(14):5497–5509. doi: 10.1063/1.471789. DOI

Kutzelnigg, W. ; Fleischer, U. ; Schindler, M. . The IGLO-Method: Ab-initio Calculation and Interpretation of NMR Chemical Shifts and Magnetic Susceptibilities; Springler, 1991.

Fukal J., Páv O., Buděšínský M., Rosenberg I., Šebera J., Sychrovský V.. Structural interpretation of the P-31 NMR chemical shifts in thiophosphate and phosphate: key effects due to spin-orbit and explicit solvent. Phys. Chem. Chem. Phys. 2019;21(19):9924–9934. doi: 10.1039/C9CP01460H. PubMed DOI

van Wullen C.. A comparison of density functional methods for the calculation of phosphorus-31 NMR chemical shifts. Phys. Chem. Chem. Phys. 2000;2(10):2137–2144. doi: 10.1039/b000461h. DOI

Ott J., Eckstein F.. P-31 NMR Spectral-Analysis of the Dodecamer D­(CGCGAATTCGCG) Biochemistry. 1985;24(10):2530–2535. doi: 10.1021/bi00331a020. DOI

Wu Z. R., Tjandra N., Bax A.. Measurement of (1)­H3′-P-31 dipolar couplings in a DNA oligonucleotide by constant-time NOESY difference spectroscopy. J. Biomol. NMR. 2001;19(4):367–370. doi: 10.1023/A:1011292803363. PubMed DOI

Tian Y., Kayatta M., Shultis K., Gonzalez A., Mueller L. J., Hatcher M. E.. NMR Investigation of Backbone Dynamics in DNA Binding Sites. J. Phys. Chem. B. 2009;113(9):2596–2603. doi: 10.1021/jp711203m. PubMed DOI PMC

Clore G. M., Murphy E. C., Gronenborn A. M., Bax A.. Determination of three-bond (1)­H3 ’-P-31 couplings in nucleic acids and protein nucleic acid complexes by quantitative J correlation spectroscopy. J. Magn. Reson. 1998;134(1):164–167. doi: 10.1006/jmre.1998.1513. PubMed DOI

Sklenář V., Bax A.. Measurement of 1H-31P NMR coupling-constants in double-stranded DNA fragments. J. Am. Chem. Soc. 1987;109(24):7525–7526. doi: 10.1021/ja00258a044. DOI

Šponer J., Bussi G., Krepl M., Banáš P., Bottaro S., Cunha R. A., Gil-Ley A., Pinamonti G., Poblete S., Jurečka P.. et al. RNA Structural Dynamics As Captured by Molecular Simulations: A Comprehensive Overview. Chem. Rev. 2018;118(8):4177–4338. doi: 10.1021/acs.chemrev.7b00427. PubMed DOI PMC